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Phil. Trans. R. Soc. B (2010) 365, 3397–3410
doi:10.1098/rstb.2010.0052
Review
Retrieving chronological age from dental
remains of early fossil hominins to
reconstruct human growth in the past
M. Christopher Dean*
Department of Cell and Developmental Biology, University College London, Gower Street,
London WC1E 6BT, UK
A chronology of dental development in Pan troglodytes is arguably the best available model with
which to compare and contrast reconstructed dental chronologies of the earliest fossil hominins.
Establishing a time scale for growth is a requirement for being able to make further comparative
observations about timing and rate during both dento-skeletal growth and brain growth. The absolute timing of anterior tooth crown and root formation appears not to reflect the period of somatic
growth. In contrast, the molar dentition best reflects changes to the total growth period. Earlier
initiation of molar mineralization, shorter crown formation times, less root length formed at gingival
emergence into functional occlusion are cumulatively expressed as earlier ages at molar eruption.
Things that are similar in modern humans and Pan, such as the total length of time taken
to form individual teeth, raise expectations that these would also have been the same in fossil
hominins. The best evidence there is from the youngest fossil hominin specimens suggests a close
resemblance to the model for Pan but also hints that Gorilla may be a better developmental
model for some. A mosaic of great ape-like features currently best describes the timing of early
hominin dental development.
Keywords: hominin evolution; dental development; incremental markings; tooth root growth;
enamel; dentine
1. BACKGROUND
The lives of all living organisms can be divided into
stages. This allows comparisons to be made between
them. There are many reasons for studying the stage
or period of growth in primates in a comparative context, which include identifying those ontogenetic
changes shared by all primates and those that are
unique to modern humans (Schultz 1937). Relative
comparisons of the stages of skeletal or dental
growth have proved to be a useful way of defining similarities and differences between both living and fossil
primates. When chronological age is known, then the
length of the phases of growth as well as the rates of
growth of individuals can be compared. Dental development is just one measure of biological maturity, but
is arguably the most stable, and it occurs over an unusually long period of time from before birth to
maturity. Besides enabling us to discover things
about the evolutionary history of our own growth
period, studies of comparative dental development
provide us with an opportunity for investigating the
biological processes that govern tooth formation from
the initial mineralization of teeth to the completion
of their roots (Swindler 1985).
*ucgacrd@ucl.ac.uk
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
Smith (1989) has shown that certain key marker
events during dental development actually correlate
better with important variables that describe lifehistory variation than any of these life-history variables
do with each other. Because of this, some tentative
inferences can be made about the way fossil primates
lived their lives compared with living primates that
go beyond simple relative dento-skeletal comparisons.
A powerful aspect of dental biology is that tooth tissues
preserve an incremental record of their growth, which
remains literally embodied within the microstructure
of enamel and dentine. This offers an opportunity to
reconstruct the period of maturation in fossil primates
and compare them in real time with living primates.
Even if it may never be possible to retrieve information
about many life-history variables from the fossil
record, it should be possible to reconstruct a time
scale for growth in the past.
2. INCREMENTAL GROWTH OF ENAMEL
AND DENTINE
The cells that form enamel and dentine (ameloblasts
and odontoblasts) secrete their matrix in a rhythmic
manner (Bromage 1991; Smith 2006; Bromage et al.
2009). A circadian rhythm in cell function is expressed
as a daily slowing of secretion during enamel and dentine formation and is still manifest in the enamel and
dentine microstructure of fully formed teeth as a
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M. C. Dean Review. Dental development in early hominins
(a)
(b)
Figure 1. Scanning electron micrograph showing perikymata
on the upper lateral incisor of MLD 11 (Au. africanus) from
Makapansgat, South Africa (a). Their spacing becomes
closer towards the cervix. Two or three regions of enamel
hypoplasia are evident indicating periods of slowed enamel
growth during tooth formation. (b) Transmitted polarized
light micrograph of enamel incremental markings seen in a
longitudinal ground section of a probable second molar fragment (Ward et al. 2001) attributed to Au. anamensis (KNMER 30748) from Allia Bay, Kenya. Coarse oblique long
period incremental markings (approx. 35 mm apart) run
from bottom left to top right and emerge at the surface
within perikymata troughs. Along prisms, that run left to
right in this image, are short period daily increments
marked by fine cross striations approximately 5 mm apart.
In this specimen, there are seven daily increments between
adjacent long period striae.
daily incremental marking (Boyde 1976, 1979, 1989,
1990a; Shinoda 1984). Thin sections of teeth prepared for histological analysis, or even polished or
naturally fractured surfaces of fossil teeth that are suitable for examination with various kinds of microscopy
(figure 1) can be used to reveal these markings in
enamel and dentine (Boyde 1989, 1990b; Dean
2000, 2006; Lacruz et al. 2006, 2008). Counts of
daily incremental markings in the teeth of individuals
with known dates of birth and death match very closely
with the number of days of life (Antoine et al. 2009).
The daily increments of enamel secretion in great
ape and fossil hominin teeth cumulate at a faster rate
than they do in modern human tooth enamel (Dean
et al. 2001). Enamel measuring 200 mm thick over
the cusp of a great ape tooth, takes on average between
55 and 65 days to form, whereas in modern humans
this takes 70 – 80 days (Dean et al. 2001; Dean 2009;
Smith et al. 2006). Daily rates of dentine formation,
however, are more similar in great apes and humans
and take between 80 and 100 days to form 200 mm
close to the root surface (Dean 2009, in press).
Another, but longer period rhythm, that also slows
dental hard tissue formation in a regular way is superimposed upon this daily rhythm (figure 1). In modern
humans this coarser more prominent marking usually
occurs every 7, 8, 9 or 10 days with a modal value of
8 days (Smith et al. 2006). Long-period incremental
markings are aligned along the original mineralizing
tissue front in both enamel and dentine. The slope
of these incremental markings, with respect to the
Phil. Trans. R. Soc. B (2010)
junction between enamel and dentine, provides a way
of estimating past rates of differentiation of new
secretory cells during tooth formation (Boyde 1963,
1964, 1990b; Shellis 1984; Dean 1985; Risnes 1986).
The rate of increase in both tooth crown height and
root height can be reconstructed by dividing increments of tooth crown length along the enamel
dentine junction (EDJ), or cement dentine junction
(CDJ) by the time intervals taken to form them
(Boyde 1963; Risnes 1986; Dean 2006, 2009). In
figure 2, consecutive 200 mm-thick increments of
enamel and dentine have been used to plot increasing
tooth height against time from the dentine horn to a
point as close to completion of the root as possible
(Dean 2009).
The number of daily increments between longperiod markings appears always to be the same in
each of the teeth of an individual but it varies between
individuals. In large samples of individuals there are
also outliers with a long-period rhythm of 6 or 11 or
even perhaps 12 days. We now know that these longperiod markings (first described by Anders Retzius
(1837) and, therefore, also referred to as Retzius
lines) occur in the enamel of other primates including
early fossil hominins (figure 1). Of 29 australopiths
examined so far, 17 (59%) showed a mean periodicity
of 7 days and of seven early Homo specimens examined
so far, two had long-period lines 7 days apart, four
were 8 days apart and one was 9 days apart (Lacruz
et al. 2008). Fossil teeth, however, are precious and
it is only rarely possible to employ partially destructive
techniques to retrieve data about their growth. Nevertheless, long-period markings also create a furrow or
trough on the external surface of permanent tooth
enamel. These so-called perikymata (waves around
the tooth) first defined by Preiswerk (1895) in ungulate enamel are well preserved on many early
hominin teeth and they can be counted with scanning
electron microscopy (figure 1) or even in obliquereflected light. They can be used to estimate enamel
formation times in fossil teeth since counts of perikymata are equivalent to counts of long-period striae
within the tooth but their periodicity may not be
known unless the internal structure of the enamel
can be visualized.
3. CONSTRUCTING A COMPARATIVE MODEL
FOR EARLY HOMININ MATURATION
Recent evidence about DNA sequence analysis and
from molecular biology suggests that modern
humans and chimpanzees are more closely related to
each other than to any other living ape (Goodman
et al. 1994; Ruvolo 1994; Bradley 2008). It is, therefore, not an unreasonable assumption that the last
common ancestor of the Pan – Homo clade had a life
history more like that of modern chimpanzees than
modern humans (Robson & Wood 2008). It is nonetheless equally likely that among the species of early
hominins there were many different life-history strategies that spanned what we know today about life
history in modern orangutans, chimpanzees, bonobos
and gorillas. One key question that we can then ask
is whether there is any evidence among early hominins
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Review. Dental development in early hominins
tooth height along EDJ (mm)
(a) 25 000
M. C. Dean
3399
(b)
20 000
15 000
10 000
5000
0
2
4
6
8
10
12
14
tooth formation time (years)
16
18
0
2
4
6
8
10
12
14
tooth formation time (years)
16
18
Figure 2. Plots of M1, M2 and M3 formation time (years) against increasing tooth height (mm) along the mesiobuccal (protoconid) EDJ (red open circles), continued along the CDJ (open blue circles) for (a) Pan troglodytes and (b) modern human
molars. The mean length (+1 s.d.) of mesiobuccal root formed at gingival emergence in free-living Pan specimens given in
Kelley et al. (2009), M1, 4.2 mm; M2, 5.2 mm; M3, 6.8 mm has been used to generate a likely range of root lengths (and
thereby corresponding ages) where molars in Pan might have emerged into the mouth (yellow filled circles). Arrows denote
the median ages of gingival emergence. The rates of crown and root growth, as well as the total tooth formation times in
modern humans and Pan, are similar but earlier initiation times compress Pan molar development into approximately 12
years rather than approximately 18 years. Distance curves for a single Gorilla M1, a short M1 fragment of KNM-ER
30749 and a longer M2 fragment of KNM-ER 30748 (both attributed to Au. anamensis, Ward et al. 2001) are superimposed
over the Pan M1 and M2 molars (filled black circles, crown; filled blue circles, root). Rates of root extension in Gorilla and
Au. anamensis are faster than in Pan.
for a period of maturation that differs from that known
today for modern chimpanzees. Another feasible question is whether there is evidence among the various
species of early hominins for any differences between
them in the timing of dental development that might
point to the presence of different life-history strategies
existing together during the first four million years of
human evolution. If this were so it might point to interesting links with climate change or diet. To answer
these questions requires a detailed knowledge of the
chronology of dental development in modern great
apes and an assessment of how early fossil hominins
do or do not compare with this. Since this is realistically only presently possible for Pan troglodytes, it
makes sense to try and construct a model that brings
together everything that is known about the timing of
dental development in P. troglodytes and use this to
examine the timing of dental development in early
hominins.
4. THE CHRONOLOGY OF DENTAL
DEVELOPMENT IN PAN TROGLODYTES
Early studies of dental development in great apes were
made on single individuals or on samples of animals
brought to zoos or acquired for comparative skeletal
collections (Keith 1899; Schultz 1924, 1935, 1940;
Zuckerman 1928; Krogman 1930; Bennejeant 1940;
Clements & Zuckerman 1953). Few of the living animals studied were actually born in captivity and so
their chronological age was rarely known. While
some early studies identified differences in the
sequence of dental eruption between great apes and
humans and also noted earlier ages for the eruption
of certain teeth, others found no differences in the
timing of dental development between great apes and
Phil. Trans. R. Soc. B (2010)
modern humans (Zuckerman 1928). In recent years
many issues have been clarified through studies on
samples of captive animals of known chronological
age. Parallel histological studies of enamel and dentine
growth in great apes have also helped to build a better
picture of the chronology of dental development in a
comparative context. What follows is a synthesis of
those studies.1
(a) Permanent tooth eruption times in Pan
In two classic longitudinal studies on chimpanzee
dental emergence, Nissen & Riesen (1945, 1964) presented the first reliable data for ages of gingival
emergence (eruption) in captive chimpanzees. They
showed that the deciduous dentition was fully emerged
into functional occlusion by approximately one year of
age (Nissen & Riesen 1945) and that for eight males
and seven females combined (Nissen & Riesen
1964), the mean ages of emergence for M1 were 3.3
years (range, 2.6 – 3.8); M2, 6.7 years (range, 5.6 –
7.8); and M3, 10.8 years (range, 9.0 – 13.6). All of
these molar eruption ages are much earlier than
those known for modern humans. Interestingly, however, the equivalent data for incisors and canines are
indistinguishable from those known for modern
humans. Mean gingival emergence ages for those
teeth are, respectively, I1: 5.7 years (range, 4.5 – 7.0);
I2: 6.4 years (range, 5.0 – 8.3); C: 9.0 years (range,
7.6 – 10.1). Kuykendall et al. (1992) in a study of 22
male and 36 female laboratory born and raised chimpanzees aged between 1 and 10 years observed
median emergence times for permanent teeth that
were rarely more than a month or two different from
the data of Nissen & Riesen (1964). One exception
was the permanent canine that in both the mandible
and maxilla erupted a year earlier at approximately
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(b) Environmental effects on dental development
in great apes
An important issue that is still not well understood is
the effect on great ape dental development of being
born and raised in captivity and perhaps more significantly, the effect of being nursed and raised by the
mother in captivity or being hand-nursed and bottlefed by humans. Zihlman et al. (2004, 2007) have presented a range of data for free-living chimpanzees that
demonstrate a slower rate of behavioural, somatic and
dental development than for captive animals. They
place M1 emergence at approximately 4 years, M2
between 6 and 8 years, canine emergence between
10 and 11 years and M3 emergence at approximately
12.5 years. Smith et al. (2006) have also illustrated a
wild-born chimpanzee aged 4.4 years (fig. 6 in Smith
et al. 2006), where M1 is still far from functional
occlusion. Phillips-Conroy & Jolly (1988) and
Kahumbu & Ely (1991) also recorded later eruption
times in free-living than in captive baboons. Even if
the degree of difference is both population- and
sample size-sensitive, some degree of difference is certainly real. Kelley et al. (2009) used the extrinsic
staining on newly emerged cusps of molar teeth to
indicate gingival emergence in wild-collected great
ape skulls. In figure 2, the mean lengths for mesiobuccal roots (+1 s.d.) measured at gingival emergence in
that study are plotted individually onto each Pan molar
root (M1, n ¼ 14; M2, n ¼ 10; M3, n ¼ 8). The age
ranges generated for these root lengths have been
used to simulate a likely range and median age of
attainment for gingival emergence in the predominantly wild-collected Pan specimens represented in
figure 3. The results are a close match with those of
Zihlman et al. (2004) for M1 and to some extent for
M2 with simulated median age of attainment of M1
at approximately 4.0 years, M2 at approximately 7.0
years and M3 at approximately 10 years. Interestingly,
they also fall close to the 32.6, 59.4 and 86 per cent of
the total time to complete dental development that
Swindler (1985) calculated for modern human molar
eruption times, assuming that this total time is
approximately 12 years in P. troglodytes. However,
with the exception of M1, these simulated median
ages of attainment for molar gingival emergence still
fall within the ranges reported for captive chimpanzees. Kelley & Schwartz (2009) have drawn attention
to the wide range of ages likely for gingival emergence
in free-living great apes but Smith et al. (2010) have
suggested that ages for gingival emergence may be
influenced more by free-living or captive rearing than
crown or root formation are.
Phil. Trans. R. Soc. B (2010)
M3
M3
M3
M3
M3
M2
M2
M2
M2
M2
8 years (range 6.5 – 8.7). Unfortunately, the age sample
of Kuykendall et al. (1992) did not extend to individuals with emerging M3s, but the general consistency
for dental emergence ages between these samples of
laboratory-raised chimpanzees is remarkable. However, these data are not so closely reflected by those
derived from a much smaller sample of free-living
chimpanzees of known chronological age originally
described by Zihlman et al. (2004) but subsequently
revisited by Smith et al. (2009, 2010).
M1
M1
M1
M1
M1
M. C. Dean Review. Dental development in early hominins
100
80
percentile
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60
40
20
0
2
3
4
5
6
7
8
9
10
11
12
age at tooth eruption (years)
Figure 3. Predicted median ages of attainment (50th percentile) for molar gingival emergence ages in Pan (M1, 4.1
years; M2, 6.9 years; M3, 10.1 years). These are derived
from the times corresponding to root lengths formed at gingival emergence shown as yellow filled circles in figure 2. The
interquartile age ranges (vertical lines) of attainment were
simulated by using 1 s.d. of root formed at gingival emergence. The median values are represented by central
vertical lines. A spread of initiation times over a lower age
range, which in reality seems likely, would, reduce these
estimates slightly.
What lies behind this difference is likely to be multifactorial but certainly to a large extent nutritional.
Lippert (1977) showed that captive hand-reared
infant apes double their birth weight by three
months, whereas mother-nursed infants do not do so
until six months. This difference persists until at
least 21 months and probably continues as a trend
into adulthood (Nissen & Riesen 1945; Fooden &
Izor 1983). Nissen & Riesen (1945), Marzke et al.
(1996) and Winkler et al. (1991) have all noted
advanced deciduous tooth emergence ages between
mother-nursed and formula-fed infant great apes.
Marzke et al. (1996) specifically made the point that
data from mother-nursed captive animals are likely to
be more directly relevant to free-living conditions
than data for hand-reared great apes. The available
data for great ape dental development needs, therefore, to be considered carefully in this light if a
model for dental development in fossil hominins is to
be realistic.
(c) Tooth initiation times, sequences
and overlaps
Swindler (1985), Anemone et al. (1991), Anemone &
Watts (1992), Kuykendall (1996) and Reid et al.
(1998) have all noted that the times for initial mineralization of the permanent incisors and canines in
Pan are very similar to those described for humans
(Kronfeld 1935) and that the sequence of mineralization is identical. Lower permanent incisors initiate
at approximately 3 –4 m after birth and canines at
4– 5 m although both earlier and later times have
been recorded (Kronfeld 1935; Anemone et al. 1991;
Kuykendall 1996; Winkler 1996; Schwartz et al.
2006). Winkler (1995) demonstrated that direct observations of tooth germs can pick up earlier initiation
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Review. Dental development in early hominins
times than radiography as Hess et al. (1932) and
Beynon et al. (1998) also observed. Reid et al. (1998)
have nonetheless noted generally similar initiation
times in Pan from histological studies for lower I1
(range, 1.8–5.6 m), lower I2 (range, 2.3–8.5 m) lower
canines (range, 4.6–6.9 m) as well as for P3 and P4
initiation (range, 1.1–1.95 years) something also
observed by Anemone et al. (1991) and Kuykendall
(1996) to between 1.4 and 1.8 years in Pan.
Understanding the differences in dental development
that exist between great apes that take approximately
12 years to grow up and modern humans that take
approximately 18 years to grow up is fundamental to
our being able to interpret juvenile fossil hominin
material. It is molar development that reflects these
somatic growth differences most closely. While the
sequence of molar initiation is also always identical in
great apes and humans (M1, M2, M3), the timing of
molar initiation has been much debated. Molar formation is drawn out in modern humans between birth
and approximately 18 years. Initiation of M1 around
birth is followed by M2 initiation at approximately 3
years and M3 initiation at approximately 8 years with
each molar then taking about 10 years to form.
Dean & Wood (1981) suggested that molar
initiation times were compressed together in great
apes (M1 close to birth, M2 at 2.5 years and M3 at
5 years) and that total molar formation times were
shorter, with M3 root formation completing between
11 and 12 years. Certainly, studies of dissected M1
germs in great apes have usually, but not always,
demonstrated three or four mineralizing cusps at
birth (Oka & Kraus 1969; Tarrant & Swindler 1972;
Moxham & Berkovitz 1974; Winkler 1996). Schwartz
et al. (2006) have described an extreme case of M1
initiation in a captive hand-raised gorilla as early as
90 days before birth. However, Anemone et al.
(1991) and Anemone (1995) in the first longitudinal
radiographic studies of dental development in captive
P. troglodytes, showed that for 16 individuals, the proposal of Dean & Wood (1981) for M2 and M3
initiation in Pan was incorrect. They demonstrated
even earlier initiation times for M2 at 1.5 years and
M3 at 3.5 – 4.0 years.
Subsequently, Kuykendall (1996) in an extensive
cross-sectional radiographic study imaged stages of
tooth formation in 118 captive chimps and reported
even younger median ages of molar initiation: M2,
1.3 years (range, 1.15– 1.48) and M3, 3.2 years
(range, 3.0 – 4.6). Despite the supposed advantage of
picking up initial mineralization of tooth germs earlier
in histological studies, Reid et al. (1998) estimated M2
initiation in Pan at between 1.7 and 1.9 years and M3
initiation between 3.6 and 3.8 years. In figure 2, for
consistency, and because for isolated teeth initiation
times can never be known, histological estimates for
molar initiation times have been used and fixed at
the average age for molar tooth types estimated in
Reid et al. (1998): M1, birth; M2, 1.75 years; M3,
3.69 years.
The issue of early molar initiation in great apes has
become confused with observations about the degree
of overlap in crown formation periods between
sequential molars. Overlap of crown formation periods
Phil. Trans. R. Soc. B (2010)
M. C. Dean
3401
has as much to do with how long or short the crown
formation period of the earlier forming molar is as it
has to do with the early or late initiation of the subsequent forming molar. Smith et al. (2006) noted the
potential effect earlier or later molar initiation might
have on eruption timing and highlighted the need to
document the degree of molar overlap in free-living
versus captive animals and in hand-reared versus
mother-nursed animals. Indeed in figure 2, a spread
of molar initiation times towards earlier ages would
reduce the simulated estimates for median emergence
times in figure 3. Winkler et al. (1996) studied a much
larger originally free-living sample of 89 orangutans
and concluded that sequential molars in orangutans
had usually begun to mineralize by the time a previous
molar had reached crown completion but that variability was too high to consistently predict that crown
initiation had always commenced prior to crown completion of a preceding molar. Smith et al. (2006) in a
histological study of Pan molars from the same individuals again noted variability in the degree of molar
overlap but that more often than not this was considerable. The effects of captive rearing, therefore, cannot
yet be resolved.
(d) Total tooth and root formation times
Kuykendall (1996) made the important observation
that the overall duration of crown and root formation
in chimpanzee permanent incisors and canines is comparable with that in modern humans. Some of the best
summary data for mean age at entering a formation
stage for modern humans (Liversidge 2009) places
apex closure for mandibular I1 (8.04 years), I2 (8.69
years), canines (12.2 years) and M1 (9.38 years) at
very close to the recorded ranges reported for Pan
(Anemone et al. 1991; Anemone 1995; Kuykendall
1996). The median values and ranges of ages for
root apex completion in Pan are: I1, 9.55 years
(range, 7.99– 10.75); I2, 9.69 years (range 8.35 –
10.75); C, approximately 12 years.
When initiation times are taken into account, total
molar formation times in Pan appear to come close to
those for modern human molars (approx. 10 years).
Data for 30 observations of mean M1 apex closure
(M1, 8.14 years, range 6.47 – 10.75 years) given in
Kuykendall (1996) and data for M2 and M3 from
Anemone et al. (1991) and Anemone (1995) also
suggest overlap in total M2 and M3 formation times
with modern humans (M2, 6.5 – 9.8 years; M3, 11 –
13 years). Kuykendall (1996), however, concluded
that, unlike incisors and canines, total molar formation
times in Pan were in fact slightly shorter than those
known for modern humans but since no longitudinal
studies exist with sufficient samples of older
animals this remains speculative. Nevertheless, the
wide range of ages reported for molar apex closure
in great apes is noteworthy. Beynon et al. (1991) illustrated a gorilla with an open M1 apex at approximately
6 years with a little more root growth to come (see also
the additional gorilla M1 in figure 2) and Schwartz
et al. (2006) yet another gorilla at the same stage but
aged only 3.2 years. These data suggest that total
molar formation times in Gorilla may be shorter than
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M. C. Dean Review. Dental development in early hominins
n=2
n=2
5.5
5.8
5.5
5.1
5.2
4.8
4.2
4.6
4.0
3.4
3.5
2.8
2.3
2.9
2.5
1.0
1.5
2.2
2.9
3.7
4.4
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6.5
1.0
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2.1
1.8
1.4
1.0
1.5
0.7
0.7
0.8
1.4
1.1
1.8
1.4
2.4
1.8
3.0
2.3
3.6
4.2
4.9
5.5
1.0
1.2
1.5
1.9
2.4
2.9
2.9
3.4
3.4
4.1
4.0
4.6
4.4
5.0
4.7
7.0
6.1
5.4
7.3
male n = 10
6.5
female n = 8
n=7
n=6
Figure 4. Anterior crown formation times in Pan troglodytes. Crown heights are divided into deciles and an average chronological age of attainment for each decile of height has been calculated from estimates of enamel formation time made from counts
of daily cross striations and long period striae in longitudinal ground sections of teeth. (Data from Reid et al. 1998, 2000;
Schwartz & Dean 2001; Schwartz et al. 2001.)
those reported for Pan but sample size and these data
for captive animals may be misleading.
(e) Crown formation times
Perhaps, the most debated aspect of great ape dental
development is the time taken to form enamel, or
crown formation time. The reason for this is that it
bears heavily on whether early fossil hominins can be
judged ‘ape-like’ or ‘human-like’ with respect to this
formation time. However, enamel formation time
may be defined differently in radiographic studies
and histological studies of tooth development
(Beynon et al. 1998; Kuykendall 2001) and an added
complication is that in histological studies, different
enamel formation times are often estimated for each
cusp of a molar tooth (Smith et al. 2006). For these
reasons and others many comparisons of enamel
formation times between modern humans and
great apes have often been either unconvincing or
incomparable (Kuykendall 2001).
With the exception of lower canines (Schwartz &
Dean 2001; Schwartz et al. 2001), the data for anterior
crown formation times in great apes is very poor.
Figure 4 summarizes what is known for a few
Phil. Trans. R. Soc. B (2010)
specimens of Pan with data taken from Reid et al.
(1998, 2000), Schwartz & Dean (2001) and Schwartz
et al. (2001). However, the data for one or two specimens of Gorilla published by Beynon et al. (1991)
and Schwartz et al. (2006) suggest crown formation
times for incisors may sometimes be as short as 2.7
years suggesting that Pan may be atypical in this
sense. Once again this raises the question of potentially
advanced dental development in captive animals or
perhaps of significant differences between Pan and
Gorilla that are currently unappreciated and in
addition, whether a Pan-like model for dental development is actually the most appropriate for early
hominins.
Knowing something about anterior crown formation
times allows us to link periodic linear hypoplastic banding patterns on anterior teeth that are common in many
Pan and Gorilla specimens collected from locations in
West Africa (Gabon, Cameroon) with two rainy seasons
each year (Skinner & Hopwood 2003). Besides being
generally under the weather in colder wetter conditions,
chimpanzees in particular are more susceptible to
increased intestinal parasite loads (Lilly et al. 2002)
since damp soil and sporadic forest floor flooding
present prefect conditions for eggs, protozoa and
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Review. Dental development in early hominins
crown and root extension rate
(mm d–1)
40
35
30
25
20
15
10
5
0
–1
0
1
2
3
4
5
6
7
8
9
tooth formation time (years)
Figure 5. Extension rates for the same sample of Pan M1s
shown in figure 2. Rates are high in the cusps of the crown
but then quickly fall to values between 4 and 8 mm d21
(see also Dean 2009). These data for 14 teeth are each
aligned (arrow) around the mean age (3.8 years) of peak
height velocity (PHV) for this sample, which displaces the
initiation and completion of tooth formation to earlier or
later ages but highlights the root spurt more clearly. The
mean chronological age and range of ages at which PHV
occurs during early root formation (3.01– 4.65 years, s.d.
0.48) broadly mirrors those ages reported for gingival
emergence in Pan M1s.
helminths to flourish. Seasonal fluctuations such as this
increase the likelihood of individuals succumbing to any
number of conditions that are known to underlie linear
enamel hypoplasias (particularly prolonged bouts of
diarrhoea or dysentery) and are a likely explanation
for many wild-collected great ape permanent canines
having, for example, 15 or so faint bands on canine
crowns that took close to 7.5 years to form enamel.
The data presented in figure 2 for molar crown
(protoconid) formation times in Pan are for slightly
bigger sample sizes than previous studies (but comparable to those of Smith et al. 2006, 2010) although they
are not based on counts or error-prone periodicities of
long period incremental markings but only on counts
of daily increments close to the EDJ: M1, 2.3 years
(range 1.78 – 2.66); M2, 2.38 years (range 1.72–
3.19); M3, 2.71 years (range 2.19 – 3.34). Mean
values for modern human (protoconid) formation
times (Reid & Dean 2005) are greater than these:
M1 (3.1 years), M2 (3.2 years) and M3 (3.27 years)
but there is overlap in the ranges (for example, see
Reid & Dean 2005 and Mahoney 2008) such that an
individual molar tooth could not always be attributed
to Pan or Homo on the basis of molar crown formation
time alone.
(f) Rates of root formation and the timing
of gingival emergence
All hominoid teeth show a pattern of change in extension rate that is dominated by an initial high rate in the
cusps of the crown but which then quickly reduces to a
more constant rate in the lateral enamel (Dean 2009).
The transition from cervical enamel formation to
cervical root formation in hominoid teeth appears to
occur without any abrupt change to the rate of
growth in tooth length (figure 5). In many teeth, but
Phil. Trans. R. Soc. B (2010)
M. C. Dean
3403
not all, the root extension rate then rises to a peak
and falls off again. In very long tooth root, there may
again be a rise in root extension rate towards apex
completion. In the small sample of Pan, M1 mesiobuccal roots plotted in figure 5, the mean age at which this
early peak in root extension rate occurs (3.8 years,
range ¼ 3.01 – 4.65 years, s.d. 0.48) is close to that
reported for gingival emergence. While this apparent
signature for gingival emergence is unlikely to be a
simple epigenetic reflection of tooth movement
through the bone, it is intuitive that root extension
rates should begin to fall off at the time of initial functional occlusion. When the data for extension rates are
aligned around this early mean peak height velocity
(PHV) rather than plotted with respect to initiation
at birth, this small rise in root extension rate is more
easily seen and not smoothed out (figure 5). For this
sample of Pan M1s, PHV is 8.7 mm d21 (range 6.1 –
10.2 mm d21). The expression of this peak in early
root growth becomes weaker distally in M2s and
M3s but is still there although it occurs later into
root formation. PHV in this sample of M2s was
6.7 mm d21 and occurred at 4.7 years (range 3.4 – 6.4
years, s.d. 0.85) into tooth formation.
(g) Summary points about dental development
in P. troglodytes
The sequence and times of initiation as well as total
tooth formation times of incisors and canines are
little different from modern humans. The ages of gingival emergence of incisors and canines are also little
different. Anterior crown formation times (with the
exception of male canines crowns which take longer
to form) are only slightly longer than average
modern human crown formation times. It is the
initiation times and eruption times of the molar dentition in modern humans that are drawn out to later ages
with prolongation of the growth period. The greatest
shift in timing appears to be in eruption times, which
can be observed both at later stages of root formation
in modern humans as well as at later ages than in Pan.
This is most marked in M3 that initiates approximately
4.5 years later in modern humans than in Pan and
which erupts into functional occlusion approximately
8 years later at close to 18 years of age. Average total
molar tooth formation times in Pan are shorter than
those in modern humans, but it only seems by between
one and two years, and while molar crown formation
times are also shorter on average, this is only by six
to nine months with overlapping ranges. It appears
(figure 2) that there is little or no difference in the
rate of growth in height of the molar crowns or roots
between Pan and modern humans. Besides these comparisons of timing in tooth formation, it may well be
that great ape teeth contain information about seasonality and perhaps even about their own eruptive history.
5. THE EVIDENCE FOR A CHRONOLOGY OF
DENTAL DEVELOPMENT IN FOSSIL HOMININS
(a) Molar eruption times
Bromage & Dean (1985) estimated the age at death of
four early hominin specimens with M1 just prior to or
at functional occlusion (Sts 24, Australopithecus
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M. C. Dean Review. Dental development in early hominins
africanus; LH 2, Au. afarensis; SK 62 and SK 63, Paranthropus robustus) to be 3.2 – 3.5 years on the basis of
perikymata counts on lower permanent incisors. Subsequently, a histological study of SK 63 (Dean et al.
1993) placed gingival emergence nearer to 4 years.
More recently, Lacruz et al. (2005) estimated M1
emergence into occlusion and age at death of the
Taung child (Au. africanus) to be between 3.73 and
3.93 years on the basis of M1 enamel formation
times and length of mesial root formed (5 – 6 mm:
Conroy & Vannier 1991a,b).
The only evidence for the status of the developing
dentition in Australopithecus of any species around
the age of M2 eruption comes from scans and radiographs of MLD 2 and Stw 327, both of which are
described as having M2s recently in functional occlusion (Skinner & Sperber 1982; Conroy & Vannier
1991a). While the M3 crypt of MLD 2 is only partially
preserved, CT scans of Stw 327 show a completed M3
crown (Conroy & Vannier 1991a). Skinner & Sperber
(1982) have drawn attention to the permanent canines
of MLD 2, which are still deep in their crypts and that
on CT scans (Conroy & Vannier 1991a) have less root
length formed than crown length. However, no histological age estimates are possible for either of these
specimens. But if the timing of canine root length
formed could be shown to match that known for
Pan, then the standards defined by Kuykendall
(1996) would provide a median age estimate of 7.6
years for MLD 2 (range 6.10– 8.75)—but this is
speculative. This age range, however, spans the range
of histological estimates for age at death of KNMWT 15000 (attributed to Homo erectus at 1.5 Ma),
where M2s were also just in functional occlusion and
where the one preserved upper M3 crown was also
just complete (Dean & Smith 2009).
(b) Molar initiation times
The approximately 3-year-old infant hominin dated to
3.3 Ma from Dikika, Ethiopia (Dik-1-1), and attributed to Au. afarensis had M1 crown complete with just
1.6 mm of mesiobuccal root formation (Alemseged
et al. 2006). The occlusal surface of the M2 crown
had already formed. This is clear evidence for early
initiation of M2 and of overlap in molar enamel formation. KNM-ER 1477, a juvenile P. boisei mandible
roughly the same chronological age, preserves the
mesial portion of what may have been a well-formed
M2 crypt. However, this is the only other potential evidence in any early hominin specimen that M2 may
already have been mineralizing at the time of M1
crown completion. The mineralizing P4 in this specimen would be expected to match M2 but this
cannot be known. A number of juvenile P. boisei or
P. robustus specimens exist with M1 at or close to
crown completion (Skinner & Sperber 1982; Dean
1987; Conroy & Vannier 1991b; Lacruz 2006). Relative
to this stage of M1 formation several of the P. robustus
specimens (SK 438, SK 64, SK 3978) appear to
show delayed premolar formation when compared
with the P. boisei specimens (KNM-ER 1477, KNMER 1820) and one explanation for this might be shorter
M1 crown formation times in P. robustus.
Phil. Trans. R. Soc. B (2010)
Unlike Pan no evidence exists to show early
initiation of M3 in fossil hominins. Stw 151, from
the late Member 4 breccia deposit at Sterkfontein, is
described as a specimen with a dentition ‘not fully distinct from that of Au. africanus but with a cranial
morphology more derived in some characters’
(Moggi-Cecchi et al. 1998). While there is a small
mandibular M3 crypt in Stw 151, it is still too small
to have accommodated a mineralizing tooth germ,
which must, therefore, have initiated after M2 crown
completion. Another specimen (SK 63, attributed to
P. robustus) contains M2 crowns that are not quite
completed but at this stage, only incipient M3 crypt
depressions in the root of the ascending mandibular
rami are present. Certainly, M3 initiation could not
have occurred prior to M2 crown completion in this
specimen.
(c) Total tooth formation times
The evidence for total anterior tooth formation times
in early hominins is lacking but what there is suggests
little difference from Pan. Median ages for combined
sexes in Pan for lower incisors at the same developmental stage (Kuykendall 1996) would estimate age
at death of Stw 151 at 4.95 years (range 4.61 – 5.22).
This is very close to the histological estimate of
5.2 – 5.3 years for this specimen (Moggi-Cecchi et al.
1998). There is then no evidence to suggest that the
timing of root formation in this early hominin was
different from that observed in Pan. Both standards
for lower lateral incisors in modern humans (8.0
years, s.d. 0.99; Liversidge 2009) and Pan (8.04
years, inter-quartile range 7.66– 8.86; Kuykendall
1996) also each give median age at death estimates
that match histological estimates for the H. erectus
youth from Nariokotome (7.6 – 8.8 years, Dean &
Smith 2009). Again this suggests that there is no evidence for any change in total incisor tooth formation
times in early hominins, but histological evidence for
ages of hominin specimens with near completed
canine roots are needed to show that this also holds
true for canines.
Stw 151 is aged histologically to between 5.2 and
5.3 years at death (Moggi-Cecchi et al. 1998). It had
M1s with one or more incomplete root apex at the
time M2, premolar and canine crowns had just completed enamel formation. This age implies that root
apex closure of M1 was at the earliest end of the age
range reported for Pan and occurred close to M2
crown completion. The end of M2 crown completion
in KNM-WT 15000 (H. erectus) was also estimated
to have completed between 4.2 and 4.9 years on the
basis of perikymata counts (Dean & Smith 2009).
Other early hominin specimens from Laetoli, LH 3
and LH 6 (attributed to Au. afarensis) consist only of
isolated teeth (White 1977). However, in both specimens, the upper M1 is at a similar stage of root apex
formation as Stw 151 and each have permanent
canine and premolar crowns close to or just completed. Close correspondence of the canine crown
perikymata counts (Stw 151 ¼ 140 and LH 6 ¼ 134)
suggests that LH 6 was close in age with the same pattern of tooth formation and the same early age for
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Review. Dental development in early hominins
M1 root completion. No M2s are preserved for
comparison in either of these specimens from Laetoli.
While speculative, a tooth fragment from Allia Bay,
Kenya, attributed to Au. anamensis (KNM-ER 30748)
may contain information about molar eruption in early
hominins. It is plotted in figure 2 as an M2, since it has
an enamel formation time (2.7 years) beyond the range
of the Pan M1s sampled here (see also Ward et al.
2001). It contains a marked early root spurt of
9.8 mm d21 at 4.2 years into tooth formation that is
within the M2 range for Pan (3.44 – 6.38 years). If
M2 initiation in Au. anamensis was close to 1.75
years, as in Pan, and if early root PHV actually reflects
the eruptive process, then this would place functional
occlusion of this tooth towards the lower end of the
range reported for M2 in Pan (5.6 – 7.8 years)
(Nissen & Riesen 1964).
A number of chronologically older hominin specimens exists with incomplete M3 roots. KNM-ER
1802 has a left M3 with just one wear facet on the protoconid and a ca 9 mm long mesial root impression in
the alveolar bone for the right M3. Sts 52 (attributed
to Au. africanus), OH5 and KNM-WT 17400 both
attributed to P. boisei, are specimens closer to dental
maturity but there is no histological evidence at all
to estimate their chronological age, only a hint from
periapical radiographs of the upper canine of OH5
that this root apex may have been recently completed
by age at death (Skinner & Sperber 1982).
(d) Crown formation times
Perikymata counts on hominin incisors and canines,
especially those attributed to Paranthropus, all point
to anterior crown formation times having been shorter
than those known for modern humans and for Pan
(Dean et al. 1993, 2001; Dean & Reid 2001). One
lower canine tooth attributed to Au. africanus
(Sts 50) has 170 perikymata suggesting a crown formation time of around four years or more (Dean &
Reid 2001) but in general the anterior teeth with the
greatest crown formation times appear to be those of
Au. anamensis and Au. afarensis. Here, canine enamel
formation times come closest to those known for
modern humans. Suwa et al. (2009a) counted 193
perikymata on the upper canine of ARA-VP-6/1 (the
holotype of Ardipithecus ramidus and a probable
male). This suggests that canine crown formation
took between 4.3 and 4.8 years in this specimen
(Suwa et al. 2009a) and so was potentially within the
range recorded for female Gorilla and Pongo, but
below the range so far recorded for female Pan canines
(Schwartz & Dean 2001). The several clear regularly
spaced hypoplastic bands illustrated on this specimen
in Suwa et al. (2009b) are reminiscent of what are
likely to be seasonally related cycles of poor growth on
living great ape canines (Skinner & Hopwood 2003).
If there were eight or nine such bands on ARA-VP-6/
1 and on other Ar. ramidus canines, this would strongly
suggest that Ar. ramidus existed in a seasonal environment with two colder wetter seasons per year.
At least seven juvenile specimens attributed to
P. boisei (KNM-ER 1477, KNM-ER 812, KNM-ER
1820, OH 30) or P. robustus (KB 5223, SK 64,
Phil. Trans. R. Soc. B (2010)
M. C. Dean
3405
SK 3978) have M1 at or close to crown completion (Skinner & Sperber 1982; Dean 1987; Conroy &
Vannier 1991b; Lacruz 2006). Some have been aged
on the basis of perikymata counts on anterior tooth
germs at between 2.5 and 3.0 years of age at death
(Dean 1987) but with some root formation. This fits
well with a histologically derived estimate of 2.4
years for M1 crown formation time in SK 63 (P. robustus) from Swartkrans, South Africa (Dean et al. 1993).
Lacruz & Ramirez Rozzi (2010) have made histological estimates of metaconid as well as total crown
formation times of two Au. afarensis molar fragments
(AL 333-52 and AL 336-1) at between 2.2 and 2.4
years. Beynon & Wood (1987) calculated a range of
molar crown formation times of 2.12 – 2.59 years in
P. boisei, while Ramirez Rozzi (1993, 1995) found
ranges of 1.93– 2.49 years for P. aethiopicus but a
greater range for enamel formation times of
P. boisei molars of all types (2.67 – 3.43 years). In
P. robustus from Kromdraai, Lacruz (2006) calculated
protoconid formation times at between 1.98 and
2.38 years and metaconid time to be near identical
(1.92 –2.37 years) but Lacruz et al. (2006) reported
protocone formation times in two Au. africanus
molars to be greater than this (M1, 2.74 years and
M2, 3.0 – 3.2 years). These latter two crown formation times are very close to mean modern
human values. In general, molar crown formation
times in early hominins are less than those in
modern humans and more similar to those of Pan
but there is considerable overlap in the ranges and
still insufficient data to compare sample mean
values statistically.
(e) Summary points about dental development
in early hominins
The cumulative rates of enamel formation follow a
similar trajectory in both Pan and early hominins (irrespective of enamel thickness and crown formation
times) that is faster than that in modern humans
(Dean et al. 2001; Lacruz et al. 2008). Estimates for
gingival emergence times for M1 in several early hominin specimens all fall within the range expected for
Pan, and in fact are all earlier than the time proposed
for free-born, free-living chimpanzees. There is, however, no direct evidence at all for ages of M2 and
M3 eruption among the earliest hominins. The evidence for molar initiation times provides only one
example (Dikika: Dik-1-1) where there is clear early
M2 initiation with respect to M1 and there is no evidence at all for M3 initiation occurring prior to
completion of M2 enamel formation in any early
hominin specimen. Total molar tooth formation
times have only been estimated in three hominin specimens, and appear to fall closest to the earlier ages
known for Pan. In contrast, those of incisors appear
similar to those observed in Pan. Anterior crown formation times are almost always consistently less than
those known for Pan with the shortest crown formation
times occurring in Paranthropus. Enamel (crown)
formation times in molars are generally within the
ranges known for Pan molars (but occasionally also
fall well within modern human ranges).
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3406
M. C. Dean Review. Dental development in early hominins
6. DISCUSSION
Constructing a chronology for dental development in
P. troglodytes as a comparative model for early hominins
is useful for a number of reasons. First, it highlights the
processes whereby dental development is likely to have
kept pace with prolongation of the period of general
growth during hominid evolution. These seem to be
confined to the sequence of molar development and
to have involved shifts in the timing of initial mineralization, slightly faster crown formation rates and
particularly, earlier times of tooth emergence into
functional occlusion. The cumulative effects of each
of these are most fully expressed in molar emergence
times, which appear to be the clearest measure of comparative development than any one of the components
that contribute to it. Estimates of M1 emergence times
in fossil hominins, as well as observations of early
molar initiation, and in some cases shorter crown formation times, resemble Pan more closely than modern
humans. However, too few specimens exist to provide
clear evidence for early initiation or earlier gingival
emergence times of M2 or M3 among australopith
specimens, although the evidence for this is a little
better in early Homo (Dean et al. 2001; Dean &
Smith 2009). The model reveals, however, that the
key indicators of a Pan-like dental maturation pattern
would include early M3 initiation with respect to M2
crown formation time and a lesser proportion of root
formed at gingival emergence in all molar tooth
types than in modern humans.
A second point to emerge from the model for Pan is
that some things appear to be little different between
Pan and Homo and, it follows, might not be expected
to differ in early hominins. Total anterior tooth formation times, and maybe also those for molars, fall
within the same range, all be it a broad range. Few
radiographic studies of molar development in Pan
have included older animals and few of the individual
plots in figure 2 extend all the way to root apex closure
and moreover, it is the distobuccal root (not the mesiobuccal root shown in figure 2) in both Pan and Gorilla
that on radiographs completes formation last (Dean &
Wood 2003). It is highly likely, therefore, that future
studies will show total molar formation times to be
equal in Pan and Homo. In this respect, the evidence
for at least three individual australopith specimens
suggests that total M1 and M2 formation time may
have been at the low end of the range reconstructed
for Pan. The plot of M2 (figure 2) attributed to Au.
anamensis (KNM-ER 30748) has a crown formation
time at the upper limit of the M2 range for Pan
(2.66 years) but a total tooth formation time of only
5.5 years (but with a little root still to form) and a
faster rate of root formation generally than in Pan
that might prove to be more typical of Gorilla. Shorter
anterior crown formation times in many australopiths
and earlier times for root completion might also turn
out to fit a Gorilla model better than a Pan model.
This mosaic of great ape-like dental development
among australopiths is perhaps what one ought to
expect given the gorilla-like anatomy of the scapula
of Dikika, Dik-1-1 (Alemseged et al. 2006) and the
gorilla-like mandibular morphology of Au. afarensis
mandibles (Rak et al. 2007).
Phil. Trans. R. Soc. B (2010)
A third observation about the chronological model
of dental development in Pan compared with that in
early hominins is that anterior tooth growth does not
appear to reflect general somatic growth. While total
anterior tooth formation times appear to be little
different, anterior crown formation times in australopiths are very variable but always shorter than in Pan
(Dean & Reid 2001; Dean et al. 2001). In this respect,
the comparative chronological model for anterior
tooth crown formation times in Pan differs completely
from that reconstructed for australopiths. Crown formation time does not relate in any simple way to
crown height (Dean 2009) within a tooth type. For
example, there is nothing to distinguish the enamel
formation times of smaller P. robustus canines from
taller canines of H. erectus (Dean et al. 1993, 2001).
The fact that both enamel thickness and anterior
tooth crown height, characters that can be broadly
linked to dietary specialization, are not tightly linked
to the time taken to form crowns is interesting. If in
fact total anterior tooth formation times are relatively
more stable than anterior tooth morphology appears
to be, then perhaps crown formation times might be
a better candidate for exploring phylogenetic relatedness among closely related species of early hominins
than tooth morphology. An interesting case in point
worth further consideration is the short time taken to
form the reduced canine crown heights of Ar. ramidus
(Suwa et al. 2009a).
All observations made so far on fossil and living
apes and on early hominins indicate that M1 eruption
times would have fallen within the simulated ranges for
free-living Pan shown in figure 3 and none appear to
fall within the ranges known for modern humans.
Interestingly, all predictions so far for M1 emergence
in fossil apes (Kelley 1997, 2002; Kelley & Smith
2003; Dean 2006) actually fall below the simulated
median age of attainment for M1 emergence predicted
in figure 3 as indeed do most estimates for early hominins. This raises questions about how different great
ape dental development in the Late Miocene might
have been to that known today for modern P. troglodytes
and how good a model modern Pan is for comparisons
with the earliest hominins. It also highlights the need
to reconstruct a chronology for dental development
in Gorilla to place that for Pan in a better modern comparative perspective. It remains a real possibility that
the chronological dental development in the earliest
hominins was more similar to that in modern Gorilla
than to modern Pan. Were this the case it would
raise very interesting issues about early hominin lifehistory strategies of the kind discussed by Kelley &
Schwartz (2009). The issue of advanced dental maturity in captive hand-reared great apes suggests that even
M1 emergence times of approximately 4.5 years predicted for H. erectus (Dean et al. 2001; Dean &
Smith 2009) would still fall comfortably within the
simulated range for wild-born chimpanzees (figure 3)
as has been suggested by Zihlman et al. (2004) but
predictions for M2 and M3 eruption of approximately
8 and approximately 14 years, respectively, in
H. erectus would not.
No convincing evidence exists for any differences in
the chronology of molar development and emergence
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Review. Dental development in early hominins
between early hominin taxa, but estimates of chronological age in specimens around 2.5 years and
younger make it clear that tooth wear was excessive
in some infant and juvenile late australopiths. Even
thicker deciduous dental enamel was insufficient to
compensate for this, resulting in extensive islands of
dentine exposure on deciduous teeth very early in
development (Aiello et al. 1991). Moggi-Cecchi et al.
(2010) describe an infant P. robustus hemi-mandible
from Drimolen (DNH-44) with an unworn erupting
Rdm2 where islands of dentine are exposed on the
Rdc and on four out of five cusps of the Rdm1, arguably within a year or so of birth. The obvious
inference that some early hominin juveniles were
taking considerable quantities of supplementary
foods at a very early age cannot, at the moment, be
extended to assuming they were also weaned early
and that interbirth intervals were relatively short in
these later australopiths, although this is one interpretation of those observations (Aiello et al. 1991; Dean
2006). Once again, there is the tantalizing suggestion
that a Gorilla-like life-history model may be a better
match for some, but not all, early hominins. Many
life-history variables in Gorilla such as age at weaning
(reviewed in Aiello et al. 1991) age at first reproduction
and interbirth interval (Watts 1991; Robson & Wood
2008; Kelley & Schwartz 2009) are reported to be
earlier than in Pan and Pongo (Wich et al. 2004).
However, a firm link with these variables and earlier
dental development remains illusive (Kelley &
Schwartz 2009; Humphrey 2010). In the future,
combined studies of tooth microstructure that put a
chronological time scale to more sophisticated
models of changing infant diets may shed more light
on early life-history events such as these during the
first four million years of human evolution (Humphrey
et al. 2008; Humphrey 2010).
I thank Alan Walker and Chris Stringer for inviting me to
contribute to this discussion meeting. Much of the
research underpinning this paper has been supported by
the Leverhulme Trust and the Royal Society through
grants to me. I thank Don Reid and Gary Schwartz for
helping with the construction of figure 4 and I am
especially grateful to Louise Humphrey, Jay Kelley, Helen
Liversidge and Holly Smith for discussions that have
helped develop some of the ideas set out here.
ENDNOTE
1
For consistency and clarity, ages given in the literature are cited here
as follows: Prenatal and postnatal ages up to 1 month are given in
days, those between 1 month and 1 year in months and those greater
than this in years.
REFERENCES
Aiello, L. C., Montgomery, C. & Dean, C. 1991 The natural
history of deciduous tooth attrition in hominoids. J. Hum.
Evol. 21, 397–412. (doi:10.1016/0047-2484(91)90114-B)
Alemseged, Z., Spoor, F., Kimbel, W. H., Bobe, R.,
Geraads, D., Reed, D. & Wynn, J. 2006 Juvenile early
hominin skeleton from Dikika, Ethiopia. Nature 443,
296 –301. (doi:10.1038/nature05047)
Anemone, R. L. 1995 Dental development in chimpanzees
of known chronological age; implications for understanding the age at death of Plio-Pleistocene hominids.
Phil. Trans. R. Soc. B (2010)
M. C. Dean
3407
In Aspects of dental biology; palaeontology, anthropology and
evolution (ed. J. Moggi-Cecchi), pp. 201–215. Florence,
Italy: International Institute for the Study of Man.
Anemone, R. L. & Watts, E. S. 1992 Dental development in
apes and humans: a comment on Simpson, Lovejoy and
Meindl (1990). J. Hum. Evol. 22, 149–153. (doi:10.
1016/0047-2484(92)90035-8)
Anemone, R. L., Watts, E. S. & Swindler, D. R. 1991 Dental
development of known age chimpanzees Pan troglodytes
(Primates, Pongidae). Am. J. Phys. Anthropol. 86,
229–241. (doi:10.1002/ajpa.1330860211)
Antoine, D., Hillson, S. & Dean, M. C. 2009 The developmental clock of dental enamel: a test for the periodicity of
prism cross-striations and an evaluation of the likely sources
of error in histological studies of this kind. J. Anat. 214,
45–55. (doi:10.1111/j.1469-7580.2008.01010.x)
Bennejeant, C. 1940 La chronologie de la dentition chez les
anthropoids. Mammalia 4, 41–45. (doi:10.1515/mamm.
1940.4.2.41)
Beynon, A. D. & Wood, B. A. 1987 Patterns and rates of
molar crown formation times in East African fossil
hominids. Nature 326, 493–496. (doi:10.1038/326493a0)
Beynon, A. D., Dean, M. C. & Reid, D. J. 1991 Histological
study on the chronology of the developing dentition
in gorilla and orangutan. Am. J. Phys. Anthropol. 86,
189–203. (doi:10.1002/ajpa.1330860208)
Beynon, A. D., Clayton, C. B., Ramirez Rozzi, F. V. & Reid,
D. J. 1998 Radiographic and histological methodologies
in estimating the chronology of crown development in
modern humans and great apes; a review, with some
applications for studies on juvenile hominids. J. Hum.
Evol. 35, 351 –370. (doi:10.1006/jhev.1998.0234)
Boyde, A. 1963 Estimation of age at death of young human
skeletal remains from incremental lines in dental enamel.
Third Int. Meeting in Forensic Immunology, Medicine,
Pathology and Toxicology, April 16th–24th, Excerpta
Medica (Int. Congress Series no. 80) Plenary Session
IIA, London, pp. 36–46.
Boyde, A. 1964 The structure and development of
mammalian enamel. PhD Thesis, University of London,
London, UK.
Boyde, A. 1976 Amelogenesis and the structure of enamel.
In Scientific foundations of dentistry (eds B. Cohen &
I. R. H. Kramer), pp. 335–352. London, UK:
W. Heinemann Medical Books Ltd.
Boyde, A. 1979 Carbonate concentration, crystal centres,
core dissolution, caries, cross striation, circadian rhythms
and compositional contrast in the SEM. J. Dent. Res. 58b,
981–983.
Boyde, A. 1989 Enamel. In Handbook of microscopic anatomy.
Vol. 2: Teeth (eds A. Oksche & L. Vollrath), pp. 309 –473.
Berlin, Germany: Springer.
Boyde, A. 1990a Developmental interpretations of dental
microstructure. In Primate life history and evolution: monographs in primatology, vol. 14 (ed. C. Jean De Rousseau),
pp. 229–267. New York, NY: Wiley-Liss Inc.
Boyde, A. 1990b Confocal optical microscopy. In Modern
microscopies: techniques and applications (eds P. J. Duke &
A. G. Michette), pp. 185– 204. New York, NY: Plenum
Press.
Bradley, B. J. 2008 Reconstructing phylogenies and phenotypes: a molecular view of human evolution. J. Anat.
212, 337–353. (doi:10.1111/j.1469-7580.2007.00840.x)
Bromage, T. G. 1991 Enamel incremental periodicity in the
pig-tailed macaque; a polychrome fluorescent labelling
study of dental hard tissues. Am. J. Phys. Anthropol. 86,
205–214. (doi:10.1002/ajpa.1330860209)
Bromage, T. G. & Dean, M. C. 1985 Re-evaluation of the
age at death of immature fossil hominids. Nature 317,
525–527. (doi:10.1038/317525a0)
Downloaded from rstb.royalsocietypublishing.org on September 20, 2010
3408
M. C. Dean Review. Dental development in early hominins
Bromage, T. G. et al. 2009 Lamellar bone is an incremental
tissue reconciling enamel rhythms, body size and
organismal life history. Cal. Tissue Int. 84, 388 –404.
(doi:10.1007/s00223-009-9221-2)
Clements, E. M. B. & Zuckerman, S. 1953 The order of
eruption of the permanent teeth in the Hominoidea.
Am. J. Phys. Anthropol. 11, 313–337. (doi:10.1002/ajpa.
1330110309)
Conroy, G. C. & Vannier, M. W. 1991a Dental development
in South African australopithecines. Part I: problems of
pattern and chronology. Am. J. Phys. Anthropol. 86,
121 –136. (doi:10.1002/ajpa.1330860204)
Conroy, G. C. & Vannier, M. W. 1991b Dental development
in South African australopithecines. Part II: dental stage
assessment. Am. J. Phys. Anthropol. 86, 137 –156.
(doi:10.1002/ajpa.1330860205)
Dean, M. C. 1985 Variation in the developing root cone
angle of the permanent mandibular teeth of modern
man and certain fossil hominids. Am. J. Phys. Anthropol.
68, 233 –238. (doi:10.1002/ajpa.1330680210)
Dean, M. C. 1987 The dental developmental status for
six East African juvenile hominids. J. Hum. Evol. 16,
197 –213. (doi:10.1016/0047-2484(87)90076-5)
Dean, M. C. 2000 Progress in understanding hominoid
dental development. J. Anat. 197, 77–101. (doi:10.
1046/j.1469-7580.2000.19710077.x)
Dean, M. C. 2006 Tooth microstructure tracks the pace of
human life history evolution. Proc. R. Soc. B 273,
2799–2808. (doi:10.1098/rspb.2006.3583)
Dean, M. C. 2009 Growth in tooth height and extension
rates in modern human and fossil hominin canines and
molars. In Frontiers of oral biology; interdisciplinary dental
morphology (eds T. Koppe, G. Meyer & K. W. Alt),
pp. 68–73. Basel, Switzerland: Karger.
Dean, M. C. In press. Daily rates of dentine formation and
root extension rates in Paranthropus boisei, KNM-ER
1817, from Koobi Fora, Kenya. In African Genesis
Symp. Proc. (eds S. Reynolds & C. Menter). South
Africa: University of Witwatersrand Press.
Dean, M. C. & Reid, D. J. 2001 Anterior tooth formation
times in Australopithecus and Paranthropus. In Twelfth
Int. Symp. on Dental Morphology (ed. A. Brooks),
pp. 135 –149. Sheffied, UK: Sheffield Academic Press.
Dean, M. C. & Smith, B. H. 2009 Growth and development
in the Nariokotome Youth, KNM-WT 15000. In The first
humans: origin of the genus Homo (eds F. E. Grine, J. C.
Fleagle & R. E. Leakey), pp. 101 –120. New York, NY:
Springer.
Dean, M. C. & Wood, B. A. 1981 Developing pongid
dentition and its use for ageing individual crania in comparative cross-sectional growth studies. Folia Primatol. 36,
111 –127. (doi:10.1159/000156011)
Dean, M. C. & Wood, B. A. 2003 A digital radiographic atlas
of the great ape skull and dentition. In Digital archives of
human paleobiology (eds L. Bondioli & R. Macchiarelli).
Milano, Italy: ADS Solutions/Consiglio Nazionale delle
Ricerche.
Dean, M. C., Beynon, A. D., Thackeray, J. F. & Macho, G.
A. 1993 Histological reconstruction of dental development and age at death of a juvenile Paranthropus robustus
specimen, SK 63, from Swartkrans, South Africa.
Am. J. Phys. Anthropol. 91, 401–419. (doi:10.1002/ajpa.
1330910402)
Dean, M. C., Leakey, M. G., Reid, D. J., Schrenk, F.,
Schwartz, G. T., Stringer, C. & Walker, A. 2001
Growth processes in teeth distinguish modern humans
from Homo erectus and earlier hominins. Nature 414,
628 –631. (doi:10.1038/414628a)
Fooden, J. & Izor, R. J. 1983 Growth curves, dental
emergence norms, and supplementary morphological
Phil. Trans. R. Soc. B (2010)
observations on known-age captive orangutans. Am,
J. Primatol. 5, 285–301. (doi:10.1002/ajp.1350050402)
Goodman, M., Bailey, W. J., Hayasaka, K., Stanhope, M. J.,
Slightom, J. & Czelusniak, J. 1994 Molecular evidence on
primate phylogeny from DNA sequences. Am. J. Phys
Anthropol. 94, 3–24. (doi:10.1002/ajpa.1330940103)
Hess, A. F., Lewis, J. M. & Roman, B. 1932 A radiographic
study of calcification of the teeth from birth to adolescence. Dent. Cosmos 74, 1053–1061.
Humphrey, L. T. 2010 Weaning behaviour in human
evolution. Semin. Cell Dev. Biol. 21, 453–461.
Humphrey, L. T., Dean, M. C., Jeffries, T. E. & Penn, M.
2008 Unlocking evidence of early diet from tooth
enamel. Proc. Natl Acad. Sci. USA 105, 6834 –6839.
(doi:10.1073/pnas.0711513105)
Kahumbu, P. & Ely, R. M. 1991 Teeth emergence in wild
olive baboons in Kenya and formulation of a dental
schedule for ageing wild baboon populations. Am. J.
Primatol. 23, 1–9. (doi:10.1002/ajp.1350230102)
Keith, A. 1899 On the chimpanzees and their relationship to
the gorilla. Proc. Zool. Soc. Lond. 67, 296 –312. (doi:10.
1111/j.1469-7998.1899.tb06859.x)
Kelley, J. 1997 Paleobiological and phylogenetic significance
of life history in Miocene hominoids. In Function,
phylogeny, and fossils: miocene hominoid evolution and adaptations (eds D. R. Begun, C. V. Ward & M. D. Rose),
pp. 173 –208. New York, NY: Plenum Press.
Kelley, J. 2002 Life history evolution in Miocene and extant
apes. In Human evolution through developmental change
(eds N. Minugh-Purvis & K. J. McNamara), pp. 223–
248. Baltimore, MD: Johns Hopkins University Press.
Kelley, J. & Schwartz, G. T. 2009 Dental development and
life history in living African and Asian apes. Proc. Natl
Acad. Sci. USA 107, 1035– 1040. (doi:10.1073/pnas.
0906206107)
Kelley, J. & Smith, T. M. 2003 Age at first molar emergence
in early Miocene Afropithecus turkanensis and life-history
evolution in the Hominoidea. J. Hum. Evol. 44,
307 –329. (doi:10.1016/S0047-2484(03)00005-8)
Kelley, J., Dean, M. C. & Ross, S. 2009 Root growth during
molar eruption in extant great apes. In Frontiers of oral
biology; interdisciplinary dental morphology (eds T. Koppe,
G. Meyer & K. W. Alt), pp. 128 –133. Basel, Switzerland:
Karger.
Krogman, W. M. 1930 Studies in growth changes in the skull
and face of anthropoids. I. The eruption of teeth in
anthropoids and Old World apes. Am. J. Anat. 46,
303 –313. (doi:10.1002/aja.1000460205)
Kronfeld, R. 1935 Development and calcification of the human
deciduous and permanent dentition. The Bur 35, 18–25.
Kuykendall, K. L. 1996 Dental development in chimpanzees
(Pan troglodytes): the timing of tooth calcification stages.
Am. J. Phys. Anthropol. 99, 135– 157. (doi:10.1002/
(SICI)1096-8644(199601)99:1,135::AID-AJPA8.3.0.
CO;2-#)
Kuykendall, K. L. 2001 On radiographic and histological
methods for assessing dental development in chimpanzees:
comments on Beynon et al. (1998) and Reid et al. (1998).
J. Hum. Evol. 40, 67–76. (doi:10.1006/jhev.2000.0445)
Kuykendall, K. L., Mahoney, C. J. & Conroy, G. C. 1992
Probit and survival analysis of tooth emergence ages
in a mixed-longitudinal sample of chimpanzees (Pan
troglodytes). Am. J. Phys. Anthropol. 89, 379–399.
(doi:10.1002/ajpa.1330890310)
Lacruz, R. S. 2006 Enamel microstructure of the hominid
KB 5223 from Kromdraai, South Africa. Am. J. Phys.
Anthropol. 132, 175 –182. (doi:10.1002/ajpa.20506)
Lacruz, R. S., Ramirez Rozzi, F. & Bromage, T. G. 2005
Dental enamel hypoplasia, age at death, and weaning in
the Taung child. S. Afr. J. Sci. 101, 567 –569.
Downloaded from rstb.royalsocietypublishing.org on September 20, 2010
Review. Dental development in early hominins
Lacruz, R. S., Ramirez Rozzi, F. & Bromage, T. G. 2006
Variation in enamel development of South African fossil
hominids. J. Hum. Evol. 51, 580 –590. (doi:10.1016/j.
jhevol.2006.05.007)
Lacruz, R. S., Dean, M. C., Ramirez Rozzi, F. & Bromage,
T. G. 2008 Megadontia, striae periodicity and patterns
of enamel secretion in Plio-Pleistocene fossil hominins.
J. Anat. 213, 148 –158. (doi:10.1111/j.1469-7580.2008.
00938.x)
Lacruz, R. S. & Ramirez Rozzi, F. V. 2010 Molar crown
development in Australopithecus afarensis. J. Hum. Evol.
58, 201– 206. (doi:10.1016/j.jhevol.2009.11.007)
Lilly, A. A., Mehlmann, P. T. & Doran, D. 2002 Intestinal
parasites in gorillas, chimpanzees and humans at
Mondika Research Site, Dzanga-Ndoki National Park,
Central African Republic. Int. J. Primatol. 23, 555–573.
(doi:10.1023/A:1014969617036)
Lippert, W. 1977 Erfahrungen bei der Aufzucht von OrangUtans (Pongo pygmaeus) im Tierpark Berlin. Der
Zoologische Garten (N.F.) 47, 209–225.
Liversidge, H. M. 2009 Permanent tooth formation as a
method of estimating age. In Frontiers of oral biology; interdisciplinary dental morphology (eds T. Koppe, G. Meyer &
K. W. Alt), pp. 153 –157. Basel, Switzerland: Karger.
Mahoney, P. 2008 Intraspecific variation in M1 enamel
development in modern humans: implications for
human evolution. J. Hum. Evol. 55, 130 –146.
Marzke, M. W., Young, D. L., Hawkey, D. E., Su, S. M.,
Fritz, J. & Alford, P. L. 1996 Comparative analysis
of weight gain, hand/wrist maturation, and dental
emergence rates in chimpanzees aged 0 –24 months
from varying captive environments. Am. J. Phys.
Anthropol. 99, 175 –190. (doi:10.1002/(SICI)10968644(199601)99:1,175::AID-AJPA10.3.0.CO;2-K)
Moggi-Cecchi, J., Tobias, P. V. & Beynon, A. D. 1998 The
mixed dentition and associated skull fragments of a juvenile
fossil hominid from Sterkfontein, South Africa. Am J.
Phys. Anthropol. 106, 425–465. (doi:10.1002/(SICI)10968644(199808)106:4,425::AID-AJPA2.3.0.CO;2-I)
Moggi-Cecchi, J., Mentor, C., Boccone, S. & Keyser, A.
2010 Early hominin dental remains from the PlioPleistocene site of Drimolen, South Africa. J. Hum.
Evol. 58, 374–405. (doi:10.1016/j.jhevol.2010.01.006)
Moxham, B. J. & Berkovitz, B. K. B. 1974 The circumnatal
dentitions of a gorilla (Gorilla gorilla) and a chimpanzee
(Pan troglodytes). J. Zool. Lond. 173, 271–276. (doi:10.
1111/j.1469-7998.1974.tb03137.x)
Nissen, H. W. & Riesen, A. H. 1945 The deciduous dentition of the chimpanzee. Growth 9, 265 –274.
Nissen, H. W. & Riesen, A. H. 1964 The eruption of the permanent dentition of chimpanzees. Am. J. Phys. Anthropol.
22, 285– 294. (doi:10.1002/ajpa.1330220315)
Oka, S. W. & Kraus, B. S. 1969 The circumnatal status
of molar crown maturation among the hominoidea.
Archs. Oral Biol. 14, 639–659. (doi:10.1016/00039969(69)90187-3)
Phillips-Conroy, J. & Jolly, C. 1988 Dental eruption
schedules of wild and captive baboons. Am. J. Primatol.
15, 17–29. (doi:10.1002/ajp.1350150104)
Preiswerk, G. 1895 Beiträge zur Kenntniss de Schmelzstrustur bei Säugethieren mit besonderer berücksichtigung
der Ungulaten. Basel, Switzerland: Akadenische
Buchhandlung. C. F. Lendorff.
Rak, Y., Ginzburg, A. & Geffen, E. 2007 Gorilla-like anatomy on Australopithecus afarensis mandibles suggests Au.
afarensis link to robust australopiths. Proc. Natl Acad.
Sci. 104, 6568–6572. (doi:10.1073/pnas.0606454104)
Ramirez Rozzi, F. V. 1993 Tooth development in East
African Paranthropus. J. Hum. Evol. 24, 429–454.
(doi:10.1006/jhev.1993.1030)
Phil. Trans. R. Soc. B (2010)
M. C. Dean
3409
Ramirez Rozzi, F. V. 1995 Time of crown formation in PlioPleistocene hominid teeth. In Aspects of dental
biology; palaeontology, anthropology and evolution. (ed. J.
Moggi-Cecchi), pp. 217 –238. Florence, Italy: International Institute for the Study of Man.
Reid, D. J. & Dean, M. C. 2005 Variation in modern human
enamel formation times. J. Hum. Evol. 50, 329– 346.
(doi:10.1016/j.jhevol.2005.09.003)
Reid, D. J., Schwartz, G. T., Dean, M. C. & Chandrasekera,
M. S. 1998 A histological reconstruction of dental development in the common chimpanzee, Pan troglodytes.
J. Hum. Evol 35, 427 –448. (doi:10.1006/jhev.1998.0248)
Reid, D. J., Hillson, S. & Dean, M. C. 2000 Defining
chronological growth standards for known fractions of
tooth crown height in primate anterior teeth.
Am. J. Phys. Anthropol. Suppl. 30, 260.
Retzius, A. 1837 Bemerkungen über den inneren Bau
der Zähne, mit besonderer Rücksicht auf dem in
Zahnknochen vorkommenden Röhrenbau. (Müllers).
Arch. Anat. Physiol. 1837, 486–566.
Risnes, S. 1986 Enamel apposition rate and the prism
periodicity in human teeth. Scand. J. Dent. Res. 94,
394–404.
Robson, S. L. & Wood, B. A. 2008 Hominin life history:
reconstruction and evolution. J. Anat. 212, 394 –425.
(doi:10.1111/j.1469-7580.2008.00867.x)
Ruvolo, M. 1994 Molecular evolutionary processes and conflicting gene trees; the hominoid case. Am. J. Phys.
Anthropol. 94, 89–113. (doi:10.1002/ajpa.1330940108)
Schultz, A. H. 1924 Growth studies on primates bearing
upon man’s evolution. Am. J. Phys. Anthropol. 7,
149–164. (doi:10.1002/ajpa.1330070218)
Schultz, A. H. 1935 Eruption and decay of the permanent
teeth of primates. Am. J. Phys. Anthropol. 19, 480–581.
Schultz, A. H. 1937 Fetal growth and development of
the rhesus monkey. Contrib. Embryol. Carneg. Inst. 26,
71–97.
Schultz, A. H. 1940 Growth and development of the
chimpanzee. Contrib. Embryol. Carneg. Inst. 28, 1–63.
Schwartz, G. T. & Dean, M. C. 2001 Ontogeny of canine
dimorphism in extant hominoids. Am. J. Phys. Anthropol.
115, 269–283. (doi:10.1002/ajpa.1081)
Schwartz, G. T., Reid, D. J. & Dean, M. C. 2001 Developmental aspects of sexual dimorphism in hominoid
canines. Int. J. Primatol. 22, 837–860. (doi:10.1023/
A:1012073601808)
Schwartz, G. T., Dean, M. C., Reid, D. J. & Zihlman, A. L.
2006 A faithful record of stressful life events preserved in
the dental developmental record of a juvenile gorilla.
Int. J. Primatol. 27, 1– 19.
Shellis, R. P. 1984 Variations in growth of the enamel crown
in human teeth and a possible relationship between
growth and enamel structure. Archs. Oral Biol. 29, 697–
705. (doi:10.1016/0003-9969(84)90175-4)
Shinoda, H. 1984 Faithful records of biological rhythms
in dental hard tissues. Chem. Today 162, 34–40.
[In Japanese.]
Skinner, M. F. & Hopwood, D. 2003 Hypothesis for the
causes and periodicity of repetitive linear enamel
hypoplasia in large, wild African (Pan troglodytes and
Gorilla gorilla) and Asian (Pongo pygmaeus) apes. Am. J.
Phys. Anthropol. 123, 216– 235. (doi:10.1002/ajpa.10314)
Skinner, M. F. & Sperber, G. H. 1982 Atlas of radiographs of
early man. New York, NY: A. R. Liss Inc.
Smith, B. H. 1989 Dental development as a measure of life
history in primates. Evolution 43, 683–688. (doi:10.2307/
2409073)
Smith, T. M. 2006 Experimental determination of the
periodicity of incremental features in enamel. J. Anat.
208, 99–113. (doi:10.1111/j.1469-7580.2006.00499.x)
Downloaded from rstb.royalsocietypublishing.org on September 20, 2010
3410
M. C. Dean Review. Dental development in early hominins
Smith, T. M., Reid, D. J., Dean, M. C., Olejniczak, A. J. &
Martin, L. B. 2006 Molar development in common
chimpanzees (Pan troglodytes). J. Hum. Evol. 52, 201 –
206. (doi:10.1016/j.jhevol.2006.09.004)
Smith, T. M., Smith, B. H. & Boesch, C. 2009 Dental
development in the Taı̈ forest chimpanzees reappraised.
Am. J. Phys. Anthropol. 138, 243.
Smith, T. M., Smith, B. H., Reid, D. J., Siedel, H., Vigilant,
L., Hublin, J.-J. & Boesch, C. 2010 Dental development
of the Taı̈ Forest chimpanzees revisited. J. Hum. Evol. 58,
363 –373. (doi:10.1016/j.jhevol.2010.02.008)
Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy,
O. C. & White, T. D. 2009a Paleobiological implications
of the Ardipithecus ramidus dentition. Science 326, 94–99.
Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy,
O. C. & White, T. D. 2009b Author’s summaries.
Paleobiological implications of the Ardipithecus ramidus
dentition. Science 326, 69. (doi:10.1126/science.1175824)
Swindler, D. R. 1985 Nonhuman primate dental development and its relation to human dental development.
In Nonhuman primate models for human growth and
development (ed. E. S. Watts), pp. 67–94. New York,
NY: A. R. Liss.
Tarrant, L. H. & Swindler, D. R. 1972 The state of
the deciduous dentition of a chimpanzee fetus (Pan
troglodytes). J. Dent. Res. 51, 677.
Ward, C. V., Leakey, M. G. & Walker, A. 2001 Morphology
of Australopithecus anamensis from Kanapoi and Allia Bay,
Kenya. J. Hum. Evol. 41, 255–368. (doi:10.1006/jhev.
2001.0507)
Watts, D. P. 1991 Mountain gorilla reproduction and sexual
behavior. Am. J. Primatol. 24, 211– 226. (doi:10.1002/
ajp.1350240307)
Phil. Trans. R. Soc. B (2010)
White, T. D. 1977 New fossil homininds from Laetolil,
Tanzania. Am. J. Phys. Anthropol. 48, 197 –229.
Wich, S. A., Utami-Atmoko, S. S., Mitra Setia, T., Rijkesen,
H. D., Schurmann, C., van Hooff, J. A. R. A. M. &
van Schaik, C. P. 2004 Life history of wild Sumatran
orangutans (Pongo abelii). J. Hum. Evol. 47, 385–398.
(doi:10.1016/j.jhevol.2004.08.006)
Winkler, L. A. 1996 A comparison of radiographic and
anatomical evidence of tooth development in infant
apes. Folia Primatol. 65, 1 –13. (doi:10.1159/000156864)
Winkler, L. A., Schwartz, J. H. & Swindler, D. R. 1991
Aspects of dental development in the orangutan
prior to eruption of the permanent dentition.
Am. J. Phys. Anthropol. 86, 255 –271. (doi:10.1002/ajpa.
1330860213)
Winkler, L. A., Schwartz, J. H. & Swindler, D. R. 1996
Development of the orang utan permanent dentition:
Assessing patterns and variation in tooth development.
Am. Phys. Anthropol. 99, 205–220. (doi:10.1002/
(SICI)1096-8644(199601)99:1,205::AID-AJPA12.3.0.
CO;2-R)
Zihlman, A., Bolter, D. & Boesch, C. 2004 Wild chimpanzee
dentition and its implications for assessing life history in
immature hominin fossils. Proc. Natl Acad. Sci. USA
101, 10541–10543. (doi:10.1073/pnas.0402635101)
Zihlman, A., Bolter, D. & Boesch, C. 2007 Skeletal and
dental growth and development in chimpanzees of the
Taı̈ National Park, Côte D’Ivoire. J. Zool. 273, 63–73.
(doi:10.1111/j.1469-7998.2007.00301.x)
Zuckerman, S. 1928 Age changes in the chimpanzee, with
special reference to growth of the brain, eruption of the
teeth and estimation of age; with a note on the Taungs
ape. Proc. Zool. Soc. Lond. 96, 1 –42.